Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils
Abstract
Many elements are scarcely soluble in aqueous conditions found in high pH environments, such as calcareous grassland soils, unless complexed to strong binding organic ligands. To overcome this limitation, some plants and microbes produce chelators that solubilize micronutrient metals such as Fe, Ni, Cu, and Zn from mineral phases. These complexes are taken up by organisms via specific membrane receptors, thereby differentially impacting the bioavailability of these metals to the plant and microbial community. Although the importance of these chelation strategies for individual organisms has been well established, little is known about which pathways coexist within rhizosphere microbiomes or how they interact and compete for metal binding. Identifying these metallophores within natural ecosystems has remained a formidable analytical challenge due to the vast diversity of compounds and poorly defined metabolic processes in complex soil matrices. Herein, we employed recently developed liquid chromatography (LC) mass spectrometry (MS) methods to characterize the speciation of water-soluble dissolved trace elements (Fe, Ni, Cu, and Zn) of soils from native tallgrass prairies in Kansas and Iowa. Both plant and fungal metallophores were identified, revealing compound-specific patterns of chelation to biologically essential metals. Numerous metabolites typically implicated in plant Fe acquisition and homeostasis, including mugineic acids,more »
- Authors:
-
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Earth and Biological Sciences Directorate
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1427526
- Alternate Identifier(s):
- OSTI ID: 1548618
- Report Number(s):
- PNNL-SA-128577
Journal ID: ISSN 0038-0717; PII: S0038071718300671
- Grant/Contract Number:
- AC05-76RL01830; 49644
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Soil Biology and Biochemistry
- Additional Journal Information:
- Journal Volume: 120; Journal Issue: C; Journal ID: ISSN 0038-0717
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Phytosiderophores; Hydroxamates; Metal exchange; High resolution mass spectrometry; Soil microbiome
Citation Formats
Boiteau, Rene M., Shaw, Jared B., Pasa-Tolic, Ljiljana, Koppenaal, David W., and Jansson, Janet K. Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils. United States: N. p., 2018.
Web. doi:10.1016/j.soilbio.2018.02.018.
Boiteau, Rene M., Shaw, Jared B., Pasa-Tolic, Ljiljana, Koppenaal, David W., & Jansson, Janet K. Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils. United States. https://doi.org/10.1016/j.soilbio.2018.02.018
Boiteau, Rene M., Shaw, Jared B., Pasa-Tolic, Ljiljana, Koppenaal, David W., and Jansson, Janet K. Thu .
"Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils". United States. https://doi.org/10.1016/j.soilbio.2018.02.018. https://www.osti.gov/servlets/purl/1427526.
@article{osti_1427526,
title = {Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils},
author = {Boiteau, Rene M. and Shaw, Jared B. and Pasa-Tolic, Ljiljana and Koppenaal, David W. and Jansson, Janet K.},
abstractNote = {Many elements are scarcely soluble in aqueous conditions found in high pH environments, such as calcareous grassland soils, unless complexed to strong binding organic ligands. To overcome this limitation, some plants and microbes produce chelators that solubilize micronutrient metals such as Fe, Ni, Cu, and Zn from mineral phases. These complexes are taken up by organisms via specific membrane receptors, thereby differentially impacting the bioavailability of these metals to the plant and microbial community. Although the importance of these chelation strategies for individual organisms has been well established, little is known about which pathways coexist within rhizosphere microbiomes or how they interact and compete for metal binding. Identifying these metallophores within natural ecosystems has remained a formidable analytical challenge due to the vast diversity of compounds and poorly defined metabolic processes in complex soil matrices. Herein, we employed recently developed liquid chromatography (LC) mass spectrometry (MS) methods to characterize the speciation of water-soluble dissolved trace elements (Fe, Ni, Cu, and Zn) of soils from native tallgrass prairies in Kansas and Iowa. Both plant and fungal metallophores were identified, revealing compound-specific patterns of chelation to biologically essential metals. Numerous metabolites typically implicated in plant Fe acquisition and homeostasis, including mugineic acids, deoxymugineic acid, nicotianamine, and hydroxynicotianamines, dominated the speciation of divalent metals such as Ni, Cu, and Zn (2–90 pmol/g soil). In contrast, the fungal siderophore ferricrocin was specific for trivalent Fe (7–32 pmol/g soil). These results define biochemical pathways that underpin the regulation of metals in the grassland rhizosphere. They also raise new questions about the competition of these compounds for metal binding and their bioavailability to different members of the rhizosphere population. In conclusion, small structural modifications result in significant differences in metal ligand selectivity, and likely impact metal uptake within the rhizosphere of grassland soils.},
doi = {10.1016/j.soilbio.2018.02.018},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 120,
place = {United States},
year = {Thu Mar 08 00:00:00 EST 2018},
month = {Thu Mar 08 00:00:00 EST 2018}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Ecology of siderophores with special reference to the fungi
journal, January 2007
- Winkelmann, Günther
- BioMetals, Vol. 20, Issue 3-4
Siderophores and the Dissolution of Iron-Bearing Minerals in Marine Systems
journal, January 2005
- Kraemer, S. M.
- Reviews in Mineralogy and Geochemistry, Vol. 59, Issue 1
A review of recent trends in electrospray ionisation–mass spectrometry for the analysis of metal–organic ligand complexes
journal, September 2010
- Keith-Roach, Miranda J.
- Analytica Chimica Acta, Vol. 678, Issue 2
Ferricrocin functions as the main intracellular iron-storage compound in mycelia ofNeurospora crassa
journal, January 1988
- Matzanke, Berthold F.; Bill, Eckard; Trautwein, Alfred X.
- Biology of Metals, Vol. 1, Issue 1
Retention of phytosiderophores by the soil solid phase – adsorption and desorption
journal, February 2016
- Walter, M.; Oburger, E.; Schindlegger, Y.
- Plant and Soil, Vol. 404, Issue 1-2
Geochemical Processes Constraining Iron Uptake in Strategy II Fe Acquisition
journal, October 2014
- Schenkeveld, W. D. C.; Schindlegger, Y.; Oburger, E.
- Environmental Science & Technology, Vol. 48, Issue 21
Siderophores in environmental research: roles and applications: Siderophores in environmental research
journal, February 2014
- Ahmed, E.; Holmström, S. J. M.
- Microbial Biotechnology, Vol. 7, Issue 3
Root exudation of phytosiderophores from soil‐grown wheat
journal, June 2014
- Oburger, Eva; Gruber, Barbara; Schindlegger, Yvonne
- New Phytologist, Vol. 203, Issue 4
Structural biology of bacterial iron uptake
journal, September 2008
- Krewulak, Karla D.; Vogel, Hans J.
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 9
Competition between micro‐organisms and roots of barley and sorghum for iron accumulated in the root apoplasm
journal, August 1995
- WirÉN, Nicolaus Von; RÖMheld, Volker; Shioiri, Takayuki
- New Phytologist, Vol. 130, Issue 4
Molecular aspects of Cu, Fe and Zn homeostasis in plants
journal, July 2006
- Grotz, Natasha; Guerinot, Mary Lou
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1763, Issue 7
An angiotensin-I converting enzyme inhibitor from buckwheat (Fagopyrum esculentum Moench) flour
journal, March 2006
- Aoyagi, Yasuo
- Phytochemistry, Vol. 67, Issue 6
Relationships between Soybean Yield, Soil pH, and Soil Carbonate Concentration
journal, July 2007
- Rogovska, Natalia P.; Blackmer, Alfred M.; Mallarino, Antonio P.
- Soil Science Society of America Journal, Vol. 71, Issue 4
Siderophores in forest soil solution
journal, November 2004
- Holmstr�m, Sara J. M.; Lundstr�m, Ulla S.; Finlay, Roger D.
- Biogeochemistry, Vol. 71, Issue 2
Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes
journal, June 2009
- Lemanceau, Philippe; Bauer, Petra; Kraemer, Stephan
- Plant and Soil, Vol. 321, Issue 1-2
Mining iron: Iron uptake and transport in plants
journal, April 2007
- Kim, Sun A.; Guerinot, Mary Lou
- FEBS Letters, Vol. 581, Issue 12
An extended siderophore suite from Synechococcus sp. PCC 7002 revealed by LC-ICPMS-ESIMS
journal, January 2015
- Boiteau, Rene M.; Repeta, Daniel J.
- Metallomics, Vol. 7, Issue 5
Siderophore Utilization by Bradyrhizobium japonicum
journal, May 1993
- Plessner, Ora; Klapatch, Taryn; Guerinot, Mary Lou
- Applied and Environmental Microbiology, Vol. 59, Issue 5
Detection and identification of ferricrocin produced by ectendomycorrhizal fungi in the genusWilcoxina
journal, July 1996
- Prabhu, Vikram; Biolchini, Peter F.; Boyer, Gregory L.
- BioMetals, Vol. 9, Issue 3
Synthesis and properties of different metal complexes of the siderophore desferriferricrocin
journal, February 2005
- Zou, Guozhang; Boyer, Gregory L.
- BioMetals, Vol. 18, Issue 1
An Extracellular Siderophore Is Required to Maintain the Mutualistic Interaction of Epichloë festucae with Lolium perenne
journal, May 2013
- Johnson, Linda J.; Koulman, Albert; Christensen, Michael
- PLoS Pathogens, Vol. 9, Issue 5
An Iron Uptake Operon Required for Proper Nodule Development in the Bradyrhizobium japonicum -Soybean Symbiosis
journal, September 2005
- Benson, Heather P.; Boncompagni, Eric; Guerinot, Mary Lou
- Molecular Plant-Microbe Interactions®, Vol. 18, Issue 9
A cross-platform toolkit for mass spectrometry and proteomics
journal, October 2012
- Chambers, Matthew C.; Maclean, Brendan; Burke, Robert
- Nature Biotechnology, Vol. 30, Issue 10
Detection of Iron Ligands in Seawater and Marine Cyanobacteria Cultures by High-Performance Liquid Chromatography–Inductively Coupled Plasma-Mass Spectrometry
journal, April 2013
- Boiteau, Rene M.; Fitzsimmons, Jessica N.; Repeta, Daniel J.
- Analytical Chemistry, Vol. 85, Issue 9
Microbial Iron Acquisition: Marine and Terrestrial Siderophores
journal, October 2009
- Sandy, Moriah; Butler, Alison
- Chemical Reviews, Vol. 109, Issue 10
Vertical distribution of fungal communities in tallgrass prairie soil
journal, September 2010
- Jumpponen, Ari; Jones, Kenneth L.; Blair, John
- Mycologia, Vol. 102, Issue 5
Review on iron availability in soil: interaction of Fe minerals, plants, and microbes
journal, November 2013
- Colombo, Claudio; Palumbo, Giuseppe; He, Ji-Zheng
- Journal of Soils and Sediments, Vol. 14, Issue 3
Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes
journal, June 2016
- White, Richard Allen; Bottos, Eric M.; Roy Chowdhury, Taniya
- mSystems, Vol. 1, Issue 3
Green Asparagus ( Asparagus officinalis ) Prevented Hypertension by an Inhibitory Effect on Angiotensin-Converting Enzyme Activity in the Kidney of Spontaneously Hypertensive Rats
journal, May 2013
- Sanae, Matsuda; Yasuo, Aoyagi
- Journal of Agricultural and Food Chemistry, Vol. 61, Issue 23
The fate of siderophores: antagonistic environmental interactions in exudate-mediated micronutrient uptake
journal, January 2015
- Harrington, James M.; Duckworth, Owen W.; Haselwandter, Kurt
- BioMetals, Vol. 28, Issue 3
Iron utilization and metabolism in plants
journal, June 2007
- Briat, Jean-François; Curie, Catherine; Gaymard, Frédéric
- Current Opinion in Plant Biology, Vol. 10, Issue 3
Trace metal transport by marine microorganisms: implications of metal coordination kinetics
journal, January 1993
- Hudson, Robert J. M.; Morel, François M. M.
- Deep Sea Research Part I: Oceanographic Research Papers, Vol. 40, Issue 1
Genotypical differences among graminaceous species in release of phytosiderophores and uptake of iron phytosiderophores
journal, April 1990
- R�mheld, V.; Marschner, H.
- Plant and Soil, Vol. 123, Issue 2
The effect of soil horizon and mineral type on the distribution of siderophores in soil
journal, April 2014
- Ahmed, Engy; Holmström, Sara J. M.
- Geochimica et Cosmochimica Acta, Vol. 131
The Ferrichrome Uptake Pathway in Pseudomonas aeruginosa Involves an Iron Release Mechanism with Acylation of the Siderophore and Recycling of the Modified Desferrichrome
journal, January 2010
- Hannauer, M.; Barda, Y.; Mislin, G. L. A.
- Journal of Bacteriology, Vol. 192, Issue 5
Nitrogen fertilization increases diversity and productivity of prairie communities used for bioenergy
journal, June 2012
- Jarchow, Meghann E.; Liebman, Matt
- GCB Bioenergy, Vol. 5, Issue 3
Femtomolar Sensitivity of Metalloregulatory Proteins Controlling Zinc Homeostasis
journal, June 2001
- Outten, C. E.
- Science, Vol. 292, Issue 5526
Functional group and fertilization affect the composition and bioenergy yields of prairie plants
journal, May 2012
- Jarchow, Meghann E.; Liebman, Matt; Rawat, Vertika
- GCB Bioenergy, Vol. 4, Issue 6
Iron oxide dissolution and solubility in the presence of siderophores
journal, March 2004
- Kraemer, Stephan M.
- Aquatic Sciences - Research Across Boundaries, Vol. 66, Issue 1
Tallgrass prairie soil fungal communities are resilient to climate change
journal, August 2014
- Jumpponen, Ari; Jones, Kenneth L.
- Fungal Ecology, Vol. 10
Coordination chemistry of microbial iron transport compounds. 24. Characterization of coprogen and ferricrocin, two ferric hydroxamate siderophores
journal, February 1983
- Wong, Geoffrey B.; Kappel, Mary J.; Raymond, Kenneth N.
- Journal of the American Chemical Society, Vol. 105, Issue 4
Quantification of Hydroxamate Siderophores in Soil Solutions of Podzolic Soil Profiles in Sweden
journal, June 2006
- Essén, Sofia A.; Bylund, Dan; Holmström, Sara J. M.
- BioMetals, Vol. 19, Issue 3
Iron Uptake and Transport in Plants: The Good, the Bad, and the Ionome
journal, October 2009
- Morrissey, Joe; Guerinot, Mary Lou
- Chemical Reviews, Vol. 109, Issue 10
Root-Secreted Nicotianamine from Arabidopsis halleri Facilitates Zinc Hypertolerance by Regulating Zinc Bioavailability
journal, August 2014
- Tsednee, M.; Yang, S. -C.; Lee, D. -C.
- PLANT PHYSIOLOGY, Vol. 166, Issue 2
Hydroxylated Phytosiderophore Species Possess an Enhanced Chelate Stability and Affinity for Iron(III)
journal, November 2000
- von Wirén, Nicolaus; Khodr, Hicham; Hider, Robert C.
- Plant Physiology, Vol. 124, Issue 3
Chemistry and biology of siderophores
journal, January 2010
- Hider, Robert C.; Kong, Xiaole
- Natural Product Reports, Vol. 27, Issue 5
Sustainable bioenergy production from marginal lands in the US Midwest
journal, January 2013
- Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong
- Nature, Vol. 493, Issue 7433
ZmYS1 Functions as a Proton-coupled Symporter for Phytosiderophore- and Nicotianamine-chelated Metals
journal, March 2004
- Schaaf, Gabriel; Ludewig, Uwe; Erenoglu, Bülent E.
- Journal of Biological Chemistry, Vol. 279, Issue 10
Experimental considerations in metal mobilization from soil by chelating ligands: The influence of soil-solution ratio and pre-equilibration – A case study on Fe acquisition by phytosiderophores
journal, February 2017
- Schenkeveld, W. D. C.; Kimber, R. L.; Walter, M.
- Science of The Total Environment, Vol. 579
Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake
journal, January 2001
- Curie, Catherine; Panaviene, Zivile; Loulergue, Clarisse
- Nature, Vol. 409, Issue 6818
Trace metal levels in edible wild fungi
journal, December 2012
- Severoglu, Z.; Sumer, S.; Yalcin, B.
- International Journal of Environmental Science and Technology, Vol. 10, Issue 2
Inventory of metal complexes circulating in plant fluids: a reliable method based on HPLC coupled with dual elemental and high‐resolution molecular mass spectrometric detection
journal, April 2016
- Flis, Paulina; Ouerdane, Laurent; Grillet, Louis
- New Phytologist, Vol. 211, Issue 3
Acquisition, Transport, and Storage of Iron by Pathogenic Fungi
journal, July 1999
- Howard, Dexter H.
- Clinical Microbiology Reviews, Vol. 12, Issue 3
Kinetic studies on the specificity of chelate-iron uptake in Aspergillus
journal, September 1975
- Wiebe, C.; Winkelmann, G.
- Journal of Bacteriology, Vol. 123, Issue 3
Stabilities of Metal Complexes of Mugineic Acids and Their Specific Affinities for Iron(III)
journal, December 1989
- Murakami, Tasuku; Ise, Kunio; Hayakawa, Minato
- Chemistry Letters, Vol. 18, Issue 12
Equilibrium and kinetic modelling of the dynamic rhizosphere
journal, December 2014
- Schenkeveld, W. D. C.; Kraemer, S. M.
- Plant and Soil, Vol. 386, Issue 1-2
A specific transporter for iron(III)-phytosiderophore in barley roots
journal, May 2006
- Murata, Yoshiko; Ma, Jian Feng; Yamaji, Naoki
- The Plant Journal, Vol. 46, Issue 4
Facing the challenges of Cu, Fe and Zn homeostasis in plants
journal, April 2009
- Palmer, Christine M.; Guerinot, Mary Lou
- Nature Chemical Biology, Vol. 5, Issue 5
Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean
journal, December 2016
- Boiteau, Rene M.; Mende, Daniel R.; Hawco, Nicholas J.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 50
Fungal siderophore metabolism with a focus on Aspergillus fumigatus
journal, January 2014
- Haas, Hubertus
- Nat. Prod. Rep., Vol. 31, Issue 10
Works referencing / citing this record:
Effects of calcium on the kinetics of a model disjunctive ligand exchange reaction: implications for dynamic trace metal ion speciation
journal, January 2019
- Rea, Laura T.; Xu, Yi; Boland, Nathan E.
- Environmental Science: Processes & Impacts, Vol. 21, Issue 1
Siderophore profiling of co-habitating soil bacteria by ultra-high resolution mass spectrometry
journal, January 2019
- Boiteau, Rene M.; Fansler, Sarah J.; Farris, Yuliya
- Metallomics, Vol. 11, Issue 1
The kinetics of siderophore‐mediated olivine dissolution
journal, February 2019
- Torres, Mark A.; Dong, Sijia; Nealson, Kenneth H.
- Geobiology, Vol. 17, Issue 4
How Plants Handle Trivalent (+3) Elements
journal, August 2019
- Poschenrieder, Charlotte; Busoms, Silvia; Barceló, Juan
- International Journal of Molecular Sciences, Vol. 20, Issue 16
How Plants Handle Trivalent (+3) Elements
journal, August 2019
- Poschenrieder, Charlotte; Busoms, Silvia; Barceló, Juan
- International Journal of Molecular Sciences, Vol. 20, Issue 16
Figures / Tables found in this record: